Nicotinic Acid Adenine Dinucleotide Phosphate (NAADP) and Ca²⁺ Mobilization

REFERENCES

• Berridge M J. Unlocking the secrets of cell signaling. Annu Rev Physiol 2005; 67: 1–21
   PubMed Web of Science ®Google Scholar
• Berridge M J, Bootman M D, Roderick H L. Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003; 4: 517–529
   PubMed Web of Science ®Google Scholar
• Clapham D E. TRP channels as cellular sensors. Nature 2003; 426: 517–524
   PubMed Web of Science ®Google Scholar
• Parekh A B, Putney J W, Jr. Store-operated calcium channels. Physiol Rev 2005; 85: 757–810
   PubMed Web of Science ®Google Scholar
• Verkhratsky A. Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 2005; 85: 201–279
   PubMed Web of Science ®Google Scholar
• Rizzuto R, Duchen M R, Pozzan T. Flirting in little space: The ER/mitochondria Ca2 + liaison. Sci STKE 2004 2004; 215, re1
   Google Scholar
• Rudolf R, Mongillo M, Rizzuto R, Pozzan T. Looking forward to seeing calcium. Nat Rev Mol Cell Biol 2003; 4: 579–586
   Google Scholar
• Clapper D L, Walseth T F, Dargie P J, Lee H C. Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J Biol Chem 1987; 262: 9561–9568
   PubMed Web of Science ®Google Scholar
• Dousa T P, Chini E N, Beers K W. Adenine nucleotide diphosphates: Emerging second messengers acting via intracellular Ca2 + release. Am J Physiol Cell Physiol 1996; 271: C1007–C1024
   PubMed Web of Science ®Google Scholar
• Galione A, Patel S, Churchill G C. NAADP-induced calcium release in sea urchin eggs. Biol Cell 2000; 92: 197–204
   PubMed Web of Science ®Google Scholar
• Lee H C. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol Rev 1997; 77: 1133–1164
   PubMed Web of Science ®Google Scholar
• Lee H C. Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu Rev Pharmacol Toxicol 2001; 41: 317–345
   PubMed Web of Science ®Google Scholar
• Lee H C, Walseth T F, Bratt G T, Hayes R N, Clapper D L. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2 +-mobilizing activity. J Biol Chem 1989; 264: 1608–1615
   PubMed Web of Science ®Google Scholar
• Lee H C, Aarhus R. A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADPribose. J Biol Chem 1995; 270: 2152–2157
   PubMed Web of Science ®Google Scholar
• Chini E N, Beers K W, Dousa T P. Nicotinate adenine dinucleotide phosphate (NAADP) triggers a specific calcium release system in sea urchin eggs. J Biol Chem 1995; 270: 3216–3223
   PubMed Web of Science ®Google Scholar
• Lee H C, Aarhus R. Structural determinants of nicotinic acid adenine dinucleotide phosphate important for its calcium-mobilizing activity. J Biol Chem 1997; 272: 20378–20383
   PubMed Web of Science ®Google Scholar
• Billington R A, Tron G C, Reichenbach S, Sorba G, Genazzani A A. Role of the nicotinic acid group in NAADP receptor selectivity. Cell Calcium 2005; 37: 81–86
   Google Scholar
• Chini E N, Dousa T P. Enzymatic synthesis and degradation of nicotinate adenine dinucletide phosphate (NAADP), a Ca2 +-releasing agonist, in rat tissues. Biochem Biophys Res Commun 1995; 209: 167–174
   PubMed Web of Science ®Google Scholar
• Lee H C, Aarhus R. Fluorescent analogs of NAADP with calcium mobilizing activity. Biochim Biophys Acta 1998; 1425: 263–271
   Google Scholar
• Walseth T F, Lee H C. Pharmacology of cyclic ADP-ribose and NAADP. Cyclic ADP-ribose and NAADP. Structures, Metabolism and Functions, H C Lee. Kluwer Academic Publisher, Dordrecht 2002
   Google Scholar
• Lee H C, Aarhus R, Gee K R, Kestner T. Caged nicotinic acid adenine dinucleotide phosphate. Synthesis and use. J Biol Chem 1997; 272: 4172–4178
   PubMed Web of Science ®Google Scholar
• Albrieux M, Lee H C, Villaz M. Calcium signaling by cyclic ADP-ribose, NAADP, and inositol trisphosphate are involved in distinct functions in Ascidian oocytes. J Biol Chem 1998; 273: 14566–14574
   Google Scholar
• Chini E N, Beers K W, Chini C C, Dousa T P. Specific modulation of cyclic-ADP ribose-induced Ca2 + release by polyamines. Am J Physiol Cell Physiol 1995; 269: C1042–C1047
   Google Scholar
• Chini E N, Liang M Y, Dousa T P. Differential effect of pH upon cyclic-ADP-ribose and nicotinate-adenine dinucleotide phosphate-induced Ca2 + release systems. Biochem J 1998; 335: 499–504
   PubMed Web of Science ®Google Scholar
• Galione A, Lee H C, Busa W B. Ca2 +-induced Ca2 + release in sea urchin egg homogenates: Modulation by cyclic ADP-ribose. Science 1991; 261: 1143–1146
   Google Scholar
• Genazzani A A, Empson R M, Galione A. Unique inactivation properties of NAADP-sensitive Ca2 + release. J Biol Chem 1996; 271: 11599–11602
   PubMed Web of Science ®Google Scholar
• Genazzani A A, Galione A. Nicotinic acid-adenine dinucleotide phosphate mobilizes Ca2 + from a thapsigargin-insensitive pool. Biochem J 1996; 315: 721–725
   PubMed Web of Science ®Google Scholar
• Genazzani A A, Galione A. A Ca2 + release mechanism gated by the novel pyridine nucleotide, NAADP. Trends Pharmacol Sci 1997; 18: 108–110
   Google Scholar
• Genazzani A A, Mezna M, Dickey D M, Michelangeli F, Walseth T F, Galione A. Pharmacological properties of the Ca2 +-release mechanism sensitive to NAADP in the sea urchin egg. Br J Pharmacol 1997; 121: 1489–1495
   PubMed Web of Science ®Google Scholar
• Chini E N, Dousa T P. Nicotinate-adenine dinucleotide phosphate-induced Ca2 +-release does not behave as a Ca2 +-induced Ca2 +-release system. Biochem J 1996; 316: 709–711
   PubMed Web of Science ®Google Scholar
• Aarhus R, Dickey D M, Graeff R M, Gee K R, Walseth T F, Lee H C. Activation and inactivation of Ca2 + release by NAADP. J Biol Chem 1996; 271: 8513–8516
   PubMedGoogle Scholar
• Cancela J M, Churchill G C, Galione A. Coordination of agonist-induced Ca2 +-signalling patterns by NAADP in pancreatic acinar cells. Nature 1999; 398: 74–76
   PubMed Web of Science ®Google Scholar
• Navazio L, Bewell M A, Siddiqua A, Dickinson G D, Galione A, Sanders D. Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate. Proc Natl Acad Sci USA 2000; 97: 8693–8698
   PubMed Web of Science ®Google Scholar
• Cancela J M, Charpentier G, Petersen O H. Co-ordination of Ca2 + signalling in mammalian cells by the new Ca2 +-releasing messenger NAADP. Pflügers Arch 2003; 446: 322–327
   Google Scholar
• Galione A, Petersen O H. The NAADP receptor: New receptors or new regulation. Mol Interv 2005; 5: 73–79
   PubMed Web of Science ®Google Scholar
• Masgrau R, Churchill G C, Morgan A J, Ashcroft S J, Galione A. NAADP: A new second messenger for glucose-induced Ca2 + responses in clonal pancreatic beta cells. Curr Biol 2003; 13: 247–251
   PubMed Web of Science ®Google Scholar
• Patel S, Churchill G C, Galione A. Coordination of Ca2 + signalling by NAADP. Trends Biochem Sci 2001; 26: 482–489
   PubMed Web of Science ®Google Scholar
• Mándi M, Tóth B, Timár Gy, Bak J. Ca2 + release triggered by NAADP in hepatocyte microsomes. Biochem J 2006; 395: 233–238
   Google Scholar
• Bak J, White P, Timár Gy, Missiaen L, Genazzani A A, Galione A. Nicotinic acid adenine dinucleotide phosphate triggers Ca2 + release from brain microsomes. Curr Biol 1999; 9: 751–754
   Google Scholar
• Bak J, Billington R A, Timár Gy, Dutton A C, Genazzani A A. NAADP receptors are present and functional in the heart. Curr Biol 2001; 11: 987–990
   Google Scholar
• Cheng J F, Yusufi A NK, Thompson M A, Chini E N, Grande J P. Nicotinic acid adenine dinucleotide phosphate: A new Ca2 + releasing agent in kidney. J Am Soc Nephrol 2001; 12: 54–60
   Google Scholar
• Berg I, Potter B V, Mayr G W, Guse A H. Nicotinic acid adenine dinucleotide phosphate (NAADP+) is an essential regulator of T-lymphocyte Ca2 +-signaling. J Cell Biol 2000; 150: 581–588
   PubMed Web of Science ®Google Scholar
• Hohenegger M, Suko J, Gscheidlinger R, Drobny H, Zidar A. Nicotinic acid-adenine dinucleotide phosphate activates the skeletal muscle ryanodine receptor. Biochem J 2002; 367: 423–431
   Google Scholar
• Yusufi A N, Cheng J, Thompson M A, Chini E N, Grande J P. Nicotinic acid-adenine dinucleotide phosphate (NAADP) elicits specific microsomal Ca2 + release from mammalian cells. Biochem J 2001; 353: 531–536
   Google Scholar
• Zhang F, Li P L. Reconstitution and characterization of an NAADP-sensitive Ca2 + release channel from liver lysosomes of rats. J Biol Chem 2007; 282: 25259–25269
   PubMed Web of Science ®Google Scholar
• Bernofsky C, Gallagher W J. Liquid chromatography of pyridine nucleotides and associated compounds and isolation of several analogs of nicotinamide adenine dinucleotide phosphate. Anal Biochem 1975; 67: 611–624
   Google Scholar
• Aarhus R, Graeff R M, Dickey D M, Walseth T F, Lee H C. ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP. J Biol Chem 1995; 270: 30327–30333
   PubMed Web of Science ®Google Scholar
• Lee H C, Aarhus R. ADP-ribosyl cyclase: An enzyme that cyclizes NAD+ into a calcium-mobilizing metabolite. Cell Regul 1991; 2: 203–209
   PubMedGoogle Scholar
• Hirata Y, Kimura N, Sato K, Ohsugi Y, Takasawa S, Okamoto H, Ishikawa J, Kaisho T, Ishihara K, Hirano T. ADP ribosyl cyclase activity of a novel bone marrow stromal cell surface molecule, BST-1. FEBS Lett 1994; 356: 244–248
   PubMed Web of Science ®Google Scholar
• Chini E N, Chini C C, Kato I, Takasawa S, Okamoto H. CD38 is the major enzyme responsible for synthesis of nicotinic acid-adenine dinucleotide phosphate in mammalian tissues. Biochem J 2002; 362: 125–130
   PubMed Web of Science ®Google Scholar
• Rusinko N, Lee H C. Widespread occurrence in animal tissues of an enzyme catalyzing the conversion of NAD+ into a cyclic metabolite with intracellular Ca2 +-mobilizing activity. J Biol Chem 1989; 264: 11725–11731
   PubMedGoogle Scholar
• Lee H C, Aarhus R. Wide distribution of an enzyme that catalyzes the hydrolysis of cyclic ADP-ribose. Biochim Biophys Acta 1993; 1164: 68–74
   PubMedGoogle Scholar
• Lee H C. Enzymatic functions and structures of CD38 and homologs. Chem Immunol 2000; 75: 39–59
   PubMed Web of Science ®Google Scholar
• States D J, Walseth T F, Lee H C. Similarities in amino acid sequences of Aplysia ADP-ribosyl cyclase and human lymphocyte antigen CD38. Trends Biochem Sci 1992; 17: 495
   PubMed Web of Science ®Google Scholar
• Liu Q, Kriksunov I A, Graeff R, Munshi C, Lee H C, Hao Q. Crystal structure of human CD38 extracellular domain. Structure 2005; 9: 1331–1339
   Google Scholar
• Kim H, Jacobson E L, Jacobson M K. Synthesis and degradation of cyclic ADP-ribose by NAD glycohydrolases. Science 1993; 261: 1330–1333
   PubMed Web of Science ®Google Scholar
• Basile G, Taglialatela-Scafati O, Damonte G, Armirotti A, Bruzzone S, Guida L, Franco L, Usai C, Fattorusso E, De Flora A, Zocchi E. ADP-ribosyl cyclases generate two unusual adenine homodinucleotides with cytotoxic activity on mammalian cells. Proc Natl Acad Sci USA 2005; 102: 14509–14514
   PubMed Web of Science ®Google Scholar
• Lee H C. Nicotinic acid adenine dinucleotide phosphate (NAADP)-mediated calcium signalling. J Biol Chem 2005; 280: 33693–33696
   PubMed Web of Science ®Google Scholar
• Churchill G C, Okada Y, Thomas J M, Genazzani A A, Patel S, Galione A. NAADP mobilizes Ca2 + from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 2002; 111: 703–708
   PubMed Web of Science ®Google Scholar
• Munshi C, Aarhus R, Graeff R, Walseth T F, Levitt D, Lee H C. Identification of the enzymatic active site of CD38 by site-directed mutagenesis. J Biol Chem 2000; 275: 21566–21571
   PubMed Web of Science ®Google Scholar
• Graeff R, Munshi C, Aarhus R, Johns M, Lee H C. A single residue at the active site of CD38 determines its NAD cyclizing and hydrolyzing activities. J Biol Chem 2001; 276: 12169–12173
   PubMed Web of Science ®Google Scholar
• Tohgo A, Munakata H, Takasawa S, Nata K, Akiyama T, Hayashi N, Okamoto H. Lysine 129 of CD38 (ADP-ribosyl cyclase/cyclic ADP-ribose hydrolase) participates in the binding of ATP to inhibit the cyclic ADP-ribose hydrolase. J Biol Chem 1997; 272: 3879–3882
   Google Scholar
• Prasad G S, McRee D E, Stura E A, Levitt D G, Lee H C, Stout C D. Crystal structure of Aplysia ADP ribosyl cyclase, a homologue of the bifunctional ectozyme CD38. Nat Struct Biol 1996; 3: 957–964
   PubMedGoogle Scholar
• Tohgo A, Takasawa S, Noguchi N, Koguma T, Nata K, Sugimoto T, Furuya Y, Yonekura H, Okamoto H. Essential cysteine residues for cyclic ADP-ribose synthesis and hydrolysis by CD38. J Biol Chem 1994; 269: 28555–28557
   PubMed Web of Science ®Google Scholar
• Zocchi E, Franco L, Guida L, Benatti U, Bargellesi A, Malavasi F, Lee H C, De Flora A. A single protein immunologically identified as CD38 displays NAD+ glycohydrolase, ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase activities at the outer surface of human erythrocytes. Biochem Biophys Res Commun 1993; 196: 1459–1465
   PubMed Web of Science ®Google Scholar
• Mehta K, Shahid U, Malavasi F. Human CD38, a cell-surface protein with multiple functions. FASEB J 1996; 10: 1408–1417
   PubMed Web of Science ®Google Scholar
• Ceni C, Muller-Steffner H, Lund F, Pochon N, Schweitzer A, De Waard M, Schuber F, Villaz M, Moutin M J. Evidence for an intracellular ADP-ribosyl cyclase/NAD+-glycohydrolase in brain from CD38-deficient mice. J Biol Chem 2003; 278: 40670–40678
   PubMed Web of Science ®Google Scholar
• Soares S, Thompson M, White T, Isbell A, Yamasaki M, Prakash Y, Lund F, Galione A, Chini E N. NAADP as a second messenger: Neither CD38 nor the base-exchange reaction are necessary for the in vivo generation of the NAADP in myometrial cells. Am J Physiol Cell Physiol 2007; 292: C227–C239
   PubMed Web of Science ®Google Scholar
• Moreschi I, Bruzzone S, Melone L, De Flora A, Zocchi E. NAADP+ synthesis from cADPRP and nicotinic acid by ADP-ribosyl cyclases. Biochem Biophys Res Commun 2006; 345: 573–580
   PubMed Web of Science ®Google Scholar
• Lerner F, Niere M, Ludwig A, Ziegler M. Structural and functional characterization of human NAD kinase. Biochem Biophys Res Commun 2001; 288: 69–74
   PubMed Web of Science ®Google Scholar
• Berridge G, Cramer R, Galione A, Patel S. Metabolism of the novel Ca2 +-mobilizing messenger nicotinic acid-adenine dinucleotide phosphate via a 2′ -specific Ca2 +-dependent phosphatase. Biochem J 2002; 365: 295–301
   PubMed Web of Science ®Google Scholar
• Berridge G, Dickinson G, Parrington J, Galione A, Patel S. Solubilization of receptors for the novel Ca2 + -mobilizing messenger, nicotinic acid adenine dinucleotide phosphate. J Biol Chem 2002; 277: 43717–43723
   Google Scholar
• Galione A, Ruas M. NAADP receptors. Cell Calcium 2005; 38: 273–280
   Google Scholar
• Billington R A, Genazzani A A. Characterization of NAADP+ binding in sea urchin eggs. Biochem Biophys Res Commun 2000; 276: 112–116
   Google Scholar
• Patel S, Churchill G C, Sharp T, Galione A. Widespread distribution of binding sites for the novel Ca2 + -mobilizing messenger, nicotinic acid adenine dinucleotide phosphate, in the brain. J Biol Chem 2000; 275: 36495–36497
   Google Scholar
• Bak J, Billington R A, Genazzani A A. Effect of luminal and extravesicular Ca2 + on NAADP binding and release properties. Biochem Biophys Res Commun 2002; 295: 806–811
   Google Scholar
• Dammermann W, Guse A H. Functional ryanodine receptor expression is required for NAADP-mediated local Ca2 + signaling in T-lymphocytes. J Biol Chem 2005; 280: 21394–21399
   Google Scholar
• Langhorst M F, Schwarzmann N, Guse A H. Ca2 + release via ryanodine receptors and Ca2 + entry: major mechanisms in NAADP-mediated Ca2 + signaling in T-lymphocytes. Cell Signal 2004; 16: 1283–1289
   Google Scholar
• Gerasimenko J V, Maruyama Y, Yano K, Dolman N J, Tepikin A V, Petersen O H, Gerasimenko O V. NAADP mobilizes Ca2 + from a thapsigargin-sensitive store in the nuclear envelope by activating ryanodine receptors. J Cell Biol 2003; 163: 271–282
   PubMed Web of Science ®Google Scholar
• Mojzisova A, Krizanova O, Zacikova L, Kominkova V, Ondrias K. Effect of nicotinic acid adenine dinucleotide phosphate on ryanodine calcium release channel in heart. Pflügers Arch 2001; 441: 674–677
   Google Scholar
• Bezin S, Charpentier G, Fossier P, Cancela J M. The Ca2 +-releasing messenger NAADP, a new player in the nervous system. J Physiol Paris 2006; 99: 111–118
   Google Scholar
• Billington R A, Thuring J W, Conway S J, Packman L, Holmes A B, Genazzani A A. Production and characterization of reduced NAADP (nicotinic acid-adenine dinucleotide phosphate). Biochem J 2004; 378: 275–280
   Google Scholar
• Schomer B, Epel D. Redox changes during fertilization and maturation of marine invertebrate eggs. Dev Biol 1998; 203: 1–11
   Google Scholar
• Schomer-Miller B, Epel D. The roles of changes in NADPH and pH during fertilization and artificial activation of the sea urchin egg. Dev Biol 1999; 216: 394–405
   Google Scholar
• Epel D, Patton C, Wallace R W, Cheung W Y. Calmodulin activates NAD kinase of sea urchin eggs: An early event of fertilization. Cell 1981; 23: 543–549
   PubMed Web of Science ®Google Scholar
• Billington R A, Ho A, Genazzani A A. Nicotinic acid adenine dinucleotide phosphate (NAADP) is present at micromolar concentrations in sea urchin spermatozoa. J Physiol 2002; 544: 107–112
   Google Scholar
• Churchill G C, O'Neill J S, Masgrau R, Patel S, Thomas J M, Genazzani A A, Galione A. Sperm deliver a new second messenger: NAADP. Curr Biol 2003; 13: 125–128
   PubMedGoogle Scholar
• Barron J T, Sasse M F, Nair A. Effect of angiotensin II on energetics, glucose metabolism and cytosolic NADH/NAD and NADPH/NADP redox in vascular smooth muscle. Mol Cell Biochem 2004; 262: 91–99
   Google Scholar
• Schumacker P T. Angiotensin II signaling in the brain: Compartmentalization of redox signaling?. Circ Res 2002; 91: 982–984
   Google Scholar
• Heidemann A C, Schipke C G, Kettenmann H. Extracellular application of nicotinic acid adenine dinucleotide phosphate induces Ca2 + signaling in astrocytes in situ. J Biol Chem 2005; 280: 35630–35640
   PubMedGoogle Scholar
• Yamasaki M, Masgrau R, Morgan A J, Churchill G C, Patel S, Ashcroft S J, Galione A. Organelle selection determines agonist-specific Ca2 + signals in pancreatic acinar and beta cells. J Biol Chem 2004; 279: 7234–7240
   PubMed Web of Science ®Google Scholar
• Yamasaki M, Thomas J M, Churchill G C, Garnham C, Lewis A M, Cancela J M, Patel S, Galione A. Role of NAADP and cADPR in the induction and maintenance of agonist-evoked Ca2 + spiking in mouse pancreatic acinar cells. Curr Biol 2005; 15: 874–878
   PubMed Web of Science ®Google Scholar
• Mitchell K J, Lai F A, Rutter G A. Ryanodine receptor type I and nicotinic acid adenine dinucleotide phosphate receptors mediate Ca2 + release from insulin-containing vesicles in living pancreatic betacells (MIN6). J Biol Chem 2003; 278: 11057–11064
   PubMed Web of Science ®Google Scholar
• Jadot M, Andrianaivo F, Dubois F, Wattiaux R. Effects of methylcyclodextrin on lysosomes. Eur J Biochem 2001; 268: 1392–1399
   Google Scholar
• Morgan A J, Galione A. NAADP induces pH changes in the lumen of acidic Ca2 + stores. Biochem J 2007; 402: 301–310
   PubMed Web of Science ®Google Scholar
• Kinnear N P, Boittin F X, Thomas J M, Galione A, Evans A M. Lysosome-sarcoplasmic reticulum junctions. A trigger zone for calcium signaling by nicotinic acid adenine dinucleotide phosphate and endothelin-1. J Biol Chem 2004; 279: 54319–54326
   PubMed Web of Science ®Google Scholar
• Brailoiu E, Hoard J L, Filipeanu C M, Brailoiu G C, Dun S L, Patel S, Dun N J. NAADP potentiates neurite outgrowth. J Biol Chem 2005; 280: 5646–5650
   PubMedGoogle Scholar
• Lim D, Kyozuka K, Gragnaniello G, Carafoli E, Santella L. NAADP+ initiates the Ca2 + response during fertilization of starfish oocytes. FASEB J 2001; 15: 2257–2267
   Google Scholar
• Cancela J M, Gerasimenko O V, Gerasimenko J V, Tepikin A V, Petersen O H. Two different but converging messenger pathways to intracellular Ca2 + release: The roles of nicotinic acid adenine dinucleotide phosphate, cyclic ADP-ribose and inositol trisphosphate. EMBO J 2000; 19: 2549–2557
   PubMed Web of Science ®Google Scholar
• Churchill G C, Galione A. NAADP induces Ca2 + oscillations via a two-pool mechanism by priming IP3- and cADPR-sensitive Ca2 + stores. EMBO J 2001; 20: 2666–2671
   PubMed Web of Science ®Google Scholar
• Churchill G C, Galione A. Spatial control of Ca2 + signaling by nicotinic acid adenine dinucleotide phosphate diffusion and gradients. J Biol Chem 2000; 275: 38687–38692
   PubMed Web of Science ®Google Scholar
• Churamani D, Carrey E A, Dickinson G D, Patel S. Determination of cellular nicotinic acid-adenine dinucleotide phosphate (NAADP) levels. Biochem J 2004; 380: 449–454
   PubMedGoogle Scholar
• Wilson H L, Galione A. Differential regulation of nicotinic acid-adenine dinucleotide phosphate and cADP-ribose production by cAMP and cGMP. Biochem J 1998; 331: 837–843
   Google Scholar
• Chini E N, De Toledo F GS. Nicotinic acid adenine dinucleotide phosphate: A new intracellular second messenger?. Am J Physiol Cell Physiol 2002; 282: C1191–C1198
   Google Scholar
• Bruzzone S, Guida L, Zocchi E, Franco L, De Flora A. Connexin 43 hemi channels mediate Ca2 +-regulated transmembrane NAD+ fluxes in intact cells. FASEB J 2001; 15: 10–12
   PubMed Web of Science ®Google Scholar
• Guida L, Bruzzone S, Sturla L, Franco L, Zocchi E, De Flora A. Equilibrative and concentrative nucleoside transporters mediate influx of extracellular cyclic ADP-ribose into 3T3 murine fibroblasts. J Biol Chem 2002; 277: 47097–47105
   PubMed Web of Science ®Google Scholar
• Billington R A, Bellomo E A, Floriddia E M, Erriquez J, Distasi C, Genazzani A A. A transport mechanism for NAADP in a rat basophilic cell line. FASEB J 2006; 20: 521–523
   PubMed Web of Science ®Google Scholar
• Liang M, Chini E N, Cheng J, Dousa T P. Synthesis of NAADP and cADPR in mitochondria. Arch Biochem Biophys 1999; 371: 317–325
   Google Scholar
• Cancela J M. Specific Ca2 + signaling evoked by cholecystokinin and acetylcholine: The roles of NAADP, cADPR, and IP3. Annu Rev Physiol 2001; 63: 99–117
   PubMed Web of Science ®Google Scholar
• Cancela J M, Van Coppenolle F, Galione A, Tepikin A V, Petersen O H. Transformation of local Ca2 + spikes to global Ca2 + transients: the combinatorial roles of multiple Ca2 + releasing messengers. EMBO J 2002; 21: 909–919
   Google Scholar
• Burdakov D, Galione A. Two neuropeptides recruit different messenger pathways to evoke Ca2 + signals in the same cell. Curr Biol 2000; 10: 993–996
   PubMed Web of Science ®Google Scholar
• Gerasimenko J V, Flowerdew S E, Voronina S G, Sukhomlin T K, Tepikin A V, Petersen O H, Gerasimenko O V. Bile acids induce Ca2 + release from both the endoplasmic reticulum and acidic intracellular calcium stores through activation of inositol trisphosphate receptors and ryanodine receptors. J Biol Chem 2006; 281: 40154–40163
   PubMed Web of Science ®Google Scholar
• Chameau P, Van De Vrede Y, Fossier P, Baux G. Ryanodine-, IP3- and NAADP-dependent calcium stores control acetylcholine release. Pflügers Arch 2001; 443: 289–296
   Google Scholar